Oviposition site choice under conflicting risks demonstrates that aquatic predators drive terrestrial egg-laying

Abstract

Laying eggs out of water was crucial to the transition to land and has evolved repeatedly in multiple animal phyla. However, testing hypotheses about this transition has been difficult because extant species only breed in one environment. The pantless treefrog, Dendropsophus ebraccatus, makes such tests possible because they lay both aquatic and arboreal eggs. Here, we test the oviposition site choices of D. ebraccatus under conflicting risks of arboreal egg desiccation and aquatic egg predation, thereby estimating the relative importance of each selective agent on reproduction. We also measured discrimination between habitats with and without predators and development of naturally laid aquatic and arboreal eggs. Aquatic embryos in nature developed faster than arboreal embryos, implying no cost to aquatic egg laying. In choice tests, D. ebraccatus avoided habitats with fish, showing that they can detect aquatic egg predators. Most importantly, D. ebraccatus laid most eggs in the water when faced with only desiccation risk, but switched to laying eggs arboreally when desiccation risk and aquatic predators were both present. This provides the first experimental evidence to our knowledge that aquatic predation risk influences non-aquatic oviposition and strongly supports the hypothesis that it was a driver of the evolution of terrestrial reproduction.

Fish embryos on land: terrestrial embryo deposition lowers oxygen uptake without altering growth or survival in the amphibious fishKryptolebias marmoratus

“…Terrestrial development allows developing embryos to exploit abundant oxygen, but also exposes embryos to the risk of desiccation (Marco, 2001;Touchon and Warkentin, 2010;Touchon and Worley, 2015). To survive in a terrestrial environment, fish embryos are typically deposited in moist environments (Frank and Leggett, 1981;Middaugh, 1981;Taylor, 1999;Martin and Swiderski, 2001;McDowall and Charteris, 2006;Martin, 2015).…”

Hierarchical decision‐making balances current and future reproductive success

“…However, we consider this not to be a major factor in our study for several reasons. First, many anuran species are able to detect aquatic predators and adjust their deposition behaviour accordingly to avoid those pools for breeding (Binckley & Resetarits, ; Touchon & Worley, ), which also has been found in A. femoralis (McKeon & Summers, ). Second, all of our analyses were performed on the drop‐off or clutch level, and thereby controlled for variable drop‐off and clutch sizes.…”

Factors influencing tadpole deposition site choice in a frog with male parental care: An experimental field study

“…We assume males would be expected to make choices that maximize offspring survival; therefore, we found it surprising that males of L. palavanensis deposit some, and in other cases all, of their tadpoles in the artificial pool with a predatory insect. The latter explanation seems unlikely given that many anuran species have the ability to detect predators present in water bodies, even when they have never been in contact with a particular predator (Touchon & Worley 2015;Downie, Livingstone & Cormack;. First, if finding larval deposition sites in a patchy environment is more pressing than the threats imposed by predators, males might choose to deposit tadpoles in any available pool despite the presence of predators.…”